TUMORS OF THE JUGULAR FORAMEN: DIAGNOSIS AND ...

CLINICAL STUDIES

TUMORS OF THE JUGULAR FORAMEN: DIAGNOSIS AND MANAGEMENT Ricardo Ramina, M.D. Neurosurgical Department, Instituto de Neurologia de Curitiba, Curitiba, and Neurosurgical Department, State University of Campinas, Campinas, Brazil

Joao Jarney Maniglia, M.D. Neurosurgical Department, Instituto de Neurologia de Curitiba, Curitiba, Brazil

Yvens Barbosa Fernandes, M.D. Neurosurgical Department, State University of Campinas, Campinas, Brazil

Jorge Rizzato Paschoal, M.D. Ear, Nose, and Throat Department, State University of Campinas, Campinas, Brazil

Leopoldo Nizan Pfeilsticker, M.D. Ear, Nose, and Throat Department, State University of Campinas, Campinas, Brazil

Maurício Coelho Neto, M.D. Neurosurgical Department, Instituto de Neurologia de Curitiba, Curitiba, Brazil Reprint requests: Ricardo Ramina, M.D., Neurological Department, Instituto de Neurologia de Curitiba, R. Goncalves Dias 713, 80240-340 Curitiba, Parana, Brazil. Email: [email protected] Received, April 19, 2004. Accepted, February 7, 2005.

NEUROSURGERY

OBJECTIVE: Jugular foramen tumors are rare cranial base lesions that present diagnostic and management difficulties. With the availability of new diagnostic procedures these tumors have been more precisely studied and questions of whether, when, and how these lesions should be treated often arise. Data from 106 consecutive patients surgically treated in the past 17 years were retrospectively analyzed to identify surgical outcomes. METHODS: The tumors were approached by a multidisciplinary team composed of neurosurgeons, ear, nose, and throat surgeons, and neuroradiologists. Hypervascular lesions were embolized 3 to 5 days before surgery. The same surgical technique was used to resect all tumors. The surgical defect was covered with vascularized myofascial flaps. The internal carotid artery was infiltrated in two patients, and a saphenous graft bypass was carried out before removal of the lesions. The facial nerve was reconstructed with nerve grafts (great auricular nerve) or XII/VII anastomosis in five cases. Postoperative radiotherapy was carried out for malignant and invasive tumors. RESULTS: Paragangliomas were the most frequent lesions, followed by schwannomas and meningiomas. Complete excision was possible in 89% of benign tumors and 80% of paragangliomas. Lower cranial nerve deficit was the most frequent complication (10 patients, 9.4%), transient in 4 patients. Facial and cochlear nerve paralysis occurred in 8 patients (7.5%). The function of the facial nerve recovered spontaneously in 3 patients. Four patients (3.7%) developed postoperative cerebrospinal fluid leakage. Four patients (3.7%) died after surgery. CONCLUSION: Radical removal of benign jugular foramen tumors is the treatment of choice and may be curative. Large lesions can be radically excised in one surgical procedure with preservation of lower cranial nerves. Cranial base reconstruction with vascularized myofascial flaps reduces the incidence of postoperative cerebrospinal fluid leakage. Damage of the lower cranial nerves is the most serious surgical complication. KEY WORDS: Cerebrospinal fluid leakage, Cranial base reconstruction, Jugular foramen tumor, Meningioma, Paraganglioma, Schwannoma, Skull base reconstruction Neurosurgery 57[ONS Suppl 1]:ONS-59–ONS-68, 2005

T

umors of the jugular foramen (JF) present special problems concerning their diagnosis and management. Important neurovascular structures at JF, cranial base, high cervical, and posterior fossa regions are involved by these lesions. Paraganglioma is the most frequent JF tumor. Its initial symptoms are, in the majority of cases, hearing loss and tinnitus. Other lesions may present paralysis of lower cranial nerves as the initial symptom. The combined expertise of neurosurgeons, ear, nose, and throat (ENT) sur-

DOI: 10.1227/01.NEU.0000163483.44754.47

geons and interventional neuroradiologists led to a better understanding of diagnosis, preoperative evaluation, and management of these patients. Surgical removal of these lesions remains a challenge, in spite of new developments of cranial base surgical techniques and interventional neuroradiology. Radical resection with preservation of cranial nerves and vessels is the aim of treatment. To achieve these goals, a precise and early diagnosis associated with adequate surgical management is mandatory. Tumor extensions into

VOLUME 57 | OPERATIVE NEUROSURGERY 1 | JULY 2005 | ONS-59

RAMINA

ET AL.

the cavernous sinus, clivus, and brainstem are often limiting factors for total removal. Since 1987, the authors have surgically treated 106 patients with tumors originating in the JF. A combined otoneurosurgical approach was used in all cases. This multidisciplinary management offers the best possibility of radical removal with preservation of the cranial nerves and vessels. Modifications of current surgical techniques based on our own experience are presented. Tumors arising in other regions, but that reached the jugular foramen, were not included in this series because the majority of these tumors present different diagnostic and surgical difficulties.

PATIENTS AND METHODS Between January 1987 and November 2004, 106 consecutive patients presented to the Neurological Institute of Curitiba (INC) and the State University of Campinas (UNICAMP) for the resection of JF lesions. There were 77 women (73%) and 29 men (27%). The most frequent initial clinical symptoms were hearing loss, tinnitus, and dysfunction of Cranial Nerves IX and X. Paragangliomas (61 cases) were the most frequent neoplasia; there were 48 women and 13 men with a mean age of 42.5 years ⫾ 12.0 (range, 18 –72 yr). In this group, four tumors were malignant with metastases to the cervical lymph nodes and two had associated common carotid artery bifurcation chemodectomas. Low cranial nerve schwannomas (18 patients) and meningiomas (10 patients) were the second most frequent tumors encountered in this series. Chordomas and chondrosarcomas (six patients), malignant tumors [carcinomas] (four patients), aneurysmic bone cysts (two patients), colesteatomas (two patients), chondroma (one patient), lymphangioma (one patient) and inflammatory granuloma (one patient) were other lesions in this series (Table 1). All patients with JF meningiomas presented initially with low cranial nerve palsy, and six cases presented with malignant lesions or tumors with malignant behavior. Eleven patients (10.3%) had undergone a previous operation. High definition computerized tomography (CT) and digital subtraction angiography (DSA) were performed for diagnosis and preoperative embolization until 1990. Since then, magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA) were used for diagnosis and follow-up of all patients. Embolization of hypervascular lesions was performed through super selective catheterization 3 to 5 days before the surgical procedure. Feeders from the external carotid artery (ECA [ascending pharyngeal, internal, maxillary, and occipital arteries]), from the internal carotid artery (ICA [carotid tympanic branches]) and vertebral artery (posteroinferior cerebellar artery) are embolized with gelatin foam (Gelfoam; Pharmacia & Upjohn, Kalamazoo, MI) and polyvinyl alcohol foam (Ivalon; Nycomed, Paris, France) particles. Balloon test occlusion was carried out in patients with large lesions surrounding the ICA and when sacrifice of this vessel was anticipated. Reconstruction of the ICA with high flow saphenous bypass was necessary in two patients. The objective of treatment was radical tumor removal in one surgical procedure with preservation of

ONS-60 | VOLUME 57 | OPERATIVE NEUROSURGERY 1 | JULY 2005

TABLE 1. Histological findings and grade of tumor resection No. of cases

Total

Subtotal

Paragangliomas

61

49a

12b

Schwannomas

18

18

0

Meningiomas

10

5

5

Aneurysmic bone cyst

2

2

0

Chondrosarcoma

4

1

3

Chordoma

2

0

2

Malignant tumors (carcinomas)

4

0

4

Cholesteatoma

2

1

1

Chondroma

1

1

0

Lymphangioma

1

1

0

Inflammatory granuloma

1

1

0

79 (74%)

27 (26%)

Histological finding

Total a b

106

Three presented with recurrence of tumor. Four malignant, three reoperation.

the cranial nerves. All patients were operated on using the same multidisciplinary surgical technique. Careful postoperative evaluation of low cranial nerve function was recorded because most patients do not tolerate acute lesion of these nerves.

Radiological Examination CT is useful for analysis of bone structures in cases of meningiomas, aneurysmic bone cysts, and chondrosarcomas. Tumor calcification and hyperostosis are well demonstrated with this examination. MRI with gadolinium showed the characteristics of a tumor, its vascularization and extension, and its relationship with neighboring structures very clearly. MRA demonstrated the tumor vascularization and venous circulation. Paragangliomas are well vascularized lesions, with heterogeneous gadolinium enhancement showing a “salt and pepper” aspect (Fig. 1). Schwannomas present a regular contour, may be cystic, enhance strongly, and, in some cases, present as “hour glass” tumors (Fig. 2). Meningiomas may present a dura tail (Fig. 3). Chordomas and chondrosarcomas are heterogeneous, presenting some areas with contrast enhancement and may cause bone destruction. DSA, routinely performed when the lesion is well vascularized, helps to study the feeding vessels, the relationship with the ICA and vertebral artery and shows associated tumors at the common carotid bifurcation. Paragangliomas are usually fed by branches of the ECA (ascending pharyngeal artery) and may invade the walls of the ICA (Fig. 4). DSA permits the evaluation of venous

www.neurosurgery-online.com

TUMORS

OF THE JUGULAR

FORAMEN

FIGURE 1. A, MRI scan with gadolinium showing a large paraganglioma of the right JF with intracranial extension. B, postoperative CT scan after total removal of the lesion. Arrows, surgical defect.

FIGURE 4. Preoperative DSA showing ICA infiltration (arrows) by a JF paraganglioma.

FIGURE 2. A, preoperative MRI scan with gadolinium showing a cystic schwannoma of the left JF. B, postoperative MRI scan after radical removal of the tumor.

FIGURE 3. A, preoperative MRI scan of a JF meningioma. Arrows, dura tail. B, postoperative MRI scan with gadolinium after total resection of the JF meningioma.

circulation and a determination of whether the jugular bulb is occluded. A hypertrophic jugular bulb causing symptoms of tinnitus and hearing loss is easily diagnosed by the venous phase of DSA. In the majority of cases, the radiological findings are typical, permitting a precise preoperative diagnosis.

Surgical Considerations Surgical Anatomy Understanding the complex surgical anatomy of the JF and its related regions is necessary to obtain adequate surgical

NEUROSURGERY

exposure. Classically, the JF is described as having two portions: the nervous part containing the glossopharyngeal nerve, the inferior petrosal sinus, and the meningeal branches of ascending pharyngeal artery and the venous part containing the sigmoid sinus, vagus, and accessory nerves. Katsuta et al. (17) divide the JF into three portions: two venous and one nervous (intrajugular). The nervous portion is localized between the two venous parts and contains Cranial Nerves IX, X, and XI. The course of the cranial nerves within the JF presents many anatomic variations. According to Sen et al. (36) the cranial nerves lie anteromedial to the jugular bulb and maintain a multifascicular histoarchitecture (particularly the Xth cranial nerve). The vagus nerve is formed by multiple fascicles and the glossopharyngeal and accessory nerves by one and two fascicles, respectively. The lower cranial nerves (IX, X, and XI) run through a septum of connective tissue in continuity with the dura mater and the pericranium. The tympanic branch of glossopharyngeal nerve (Jacobson’s nerve) and the auricular branch of vagus nerve (Arnold’s nerve) cross the JF. Dissection of the neck should identify the following muscles, vessels and nerves. Muscles: anterior border of the sternocleidomastoid muscle (SCM), the digastric, splenius capitis, obliquus capitis superior and inferior, and splenius cervicis muscles. Vessels: common carotid, ECA with its branches and ICAs, vertebral artery at the cranial cervical junction, common facial vein, external and internal jugular veins. Nerves: greater auricular nerve; Cranial Nerves X, XI, and XII; and the sympathetic trunk. The facial nerve is exposed at the stylomastoid foramen region after identification of the mastoid tip posteriorly, the “pointer” superiorly, and the posterior belly of the digastric muscle inferiorly (Fig. 5). In most patients, the XIth cranial nerve courses lateral to the internal jugular vein and has to be transposed to remove the extracranial portion of the lesion. Important anatomic structures of the temporal bone related to the surgical approach are: the sigmoid, transverse,


RAMINA

ET AL.

FIGURE 6. Skin incision (red line) and mastoid tip (arrow).

Technique of Cranial Base Reconstruction FIGURE 5. Anatomic specimen demonstrating the facial nerve (VII) in the parotid region and mastoid (arrows). M.T., mastoid tip; S.S., sigmoid sinus.

superior and inferior petrosal sinuses, the mastoid cells and its antrum, the semicircular canals, the ossicles, the facial nerve canal, and the tympanic bone. The ICA runs medial to the tympanic bone and gives off the carotid-tympanicum branches. The anatomy of the intradural portion of the JF includes the caudal Cranial Nerves IX, X, and XI (with its spinal portion), Cranial Nerves VII and VIII, the vertebral, posteroinferior and anteroinferior cerebellar arteries, the lower brainstem, and the upper cervical cord.

Surgical Procedure Position of Patient and Skin Incision All patients in this series were operated on in a dorsal position with the head turned 45 degrees to the opposite side. Intraoperative monitoring of the facial nerve was performed in most cases. Care was taken to not compress the opposite jugular vein. The long duration of the operation required protection of all contact areas by use of foam pads or water bags. A C-shaped skin incision was made starting in the temporal region, then circumscribing the ear and reaching the anterior border of the SCM (Fig. 6). The scalp was folded anteriorly. The great auricular nerve and the osteocartilaginous junction of the external auditory canal were exposed. The great auricular nerve was cut just behind its bifurcation over the parotid gland and was used as a graft to reconstruct the facial nerve when necessary. The external auditory canal was cut at the osteocartilaginous junction in cases in which there was an anterior extension of the lesion and when hearing was already lost. The external auditory canal was sutured, and a fascia or muscle flap was turned over the suture line to avoid creating a cerebrospinal fluid (CSF) fistula.


To obtain closure of the wound in three layers, a new surgical technique was developed using vascularized tissues and fascia muscle flaps. This strategy provides very good cosmetic results, without the use of abdominal fat grafts. The first layer is the dura mater. If possible, watertight dura closure is performed. When resection of the infiltrated dura is necessary, a graft of the temporalis fascia is used to close the defect. Fibrin glue is used to reinforce the suture line of the dura. The next layer is a vascularized muscle temporalis flap. Approximately half of this muscle is incised, dissected, and turned down at the end of surgery to cover the dura. This muscle flap is sutured in the cervical and parotid fasciae, filling the entire mastoid cavity to produce a better cosmetic result. The myofascial (temporalis fascia, cervical fascia, and SCM) flap is the third layer. The temporalis muscle fascia is incised in the middle portion of the temporal region and dissected inferiorly to the temporal line. The cervical fascia is cut posterior to the external auditory canal, mastoid tip, and over the SCM. The insertion of the SCM is removed from the mastoid and a vascularized myofascial flap formed by the temporalis muscle fascia, the cervical fascia, and the SCM is turned posteriorly and inferiorly. This flap is secured with sutures in the temporalis fascia, the parotid, and cervical fascia. It is turned back to cover the temporalis muscle flap and the entire surgical field (Fig. 7).

Neck Dissection Neck dissection is the next step of the operation (Fig. 8). The anterior border of the SCM is clearly identified. The external jugular vein is ligated with suture and ligature and is cut. The major vessels of the neck (common carotid artery, ICA, and ECA [and their branches], and the internal jugular vein) are dissected. Identification of the digastric muscle is an important parameter for dissection of Cranial Nerves XII and VII. The XIIth cranial nerve crosses the ECA inferior to the digastric muscle. The accessory nerve runs laterally to the jugular vein in the majority of cases and enters the upper portion of the SCM. The vagus nerve and the sympathetic trunk run lateroinferior to the common carotid artery. The identification of


TUMORS

OF THE JUGULAR

FORAMEN

the nerve was removed from its bony canal. Resection of the facial nerve is performed when the nerve is infiltrated and reconstruction is accomplished with grafts from great auricular or sural nerves.

Temporal Bone Dissection

FIGURE 7. Cranial base reconstruction with myofascial flaps. A, rotation of the temporalis muscle (T.M.) to cover the mastoidectomy and craniotomy. B, the temporalis fascia (T.F.), craniocervical fascia (C.C.F.), and sternocleidomastoid muscle (S.T.M.) are sutured back to cover the entire surgical defect.

Temporal bone dissection is the next step. Radical mastoidectomy is performed with the identification of the facial nerve canal, the labyrinth, mastoid antrum, ossicles, and the sinodural angle. The sigmoid sinus is exposed from the superior petrosal sinus to the jugular bulb. The sigmoid sinus and the jugular bulb are completely skeletonized (Fig. 9). The dura anterior to the sigmoid sinus is dissected and the retrofacial mastoid cells are removed. A meatoplasty with opening of the posterior and anterior walls of the external auditory meatus and removal of the tympanic membrane is carried out. Tumors within the ear, eustachian tube, and mastoid cells, are removed. The removal of the tympanic bone exposes the ICA (distal control) and allows the possibility of bipolar coagulation of the carotid-tympanic branches.

Craniectomy A small craniectomy exposing the posterior fossa dura (diameter, 3 cm) is cut. Its limits are the transverse and sigmoid sinuses. The emissary mastoid vein is coagulated and cut and the sigmoid sinus is totally exposed. After removal of the lateral process of C1, the JF is widely opened, communicating its cervical portion with the cranial.

Extradural Tumor Removal Small dura incisions are performed in front of and behind the sigmoid sinus, below the superior petrosal sinus. The sigmoid sinus is ligated with two stitches. The internal jugular

FIGURE 8. Neck dissection showing a paraganglioma (TU) in the JF and ear. I.J.V., internal jugular vein; XI and XII, cranial nerves; M.T., mastoid tip.

vertebral artery is an important surgical step, especially in the case of infiltrative tumors. The vertebral artery is identified at the cranial base after dissection of the lateral process of C1 and the superior and inferior oblique muscles.

Facial Nerve Management The facial nerve is dissected in the stylomastoid and parotid region using the mastoid tip, the posterior belly of the digastric muscle, the “pointer,” and the tympanomastoid suture as parameters (Fig. 5). According to our experience, if this nerve is not infiltrated by the tumor, it is not necessary to remove it from its bony canal. The tumor can be removed anterior and posterior to the facial canal. This technique avoids postoperative facial palsy, which occurs in almost all patients in whom

NEUROSURGERY

FIGURE 9. Radical mastoidectomy and craniotomy. Tumor in the jugular bulb (TU). S.S., sigmoid sinus; VA, vertebral artery; C1, lateral process of C1; XI, cranial nerve; I.J.V., internal jugular vein; G.A.N., great auricular nerve.


RAMINA

ET AL.

vein is double ligated and cut. Resection of the extradural portion of the lesion with the ligated internal jugular vein is performed by opening the posterior wall of the sigmoid sinus and dissection from the vertebral artery. Bleeding from the inferior petrosal sinus may occur. This sinus is packed with Gelfoam or Surgicel (Ethicon, Inc., Somerville, NJ) after complete tumor removal from JF. Anterior extradural extension into the tympanic bone compressing the ICA is exposed and totally resected. In cases of schwannomas with small extension to the cervical region, tumor removal is accomplished without ligation of the sigmoid sinus.

Intradural Tumor Removal The dura mater is incised in the medial wall of sigmoid sinus. Minimal cerebellar retraction is needed to open the cerebellomedularis cistern, exposing the intradural JF region. When the intradural portion of the lesion is not very large, the caudal cranial nerves are identified intra- and extradurally and are dissected from the tumor (Fig. 10). Cranial Nerves VII and VIII are identified. Shrinkage of the lesion is performed with bipolar coagulation and the tumor is completely removed (Fig. 10). Identification of cranial nerves is difficult in large lesions compressing the brainstem. In these cases, stepby-step shrinkage of the tumor mass and intracapsular tumor removal permits the identification of the cranial nerves at the brainstem. Intraoperative monitoring of the caudal cranial nerves and facial nerve is routine and very useful for this dissection. Usually some fascicles of Cranial Nerves IX, X and XI are infiltrated and have to be resected in order to achieve total removal. Removal of the tumor, infiltrated bone, and dura mater is attempted in all cases. Malignant or aggressive tumors show no clear cleavage planes and total removal is not possible in these cases. Wound closure is performed, as described above, by turning back the fascia and muscle flaps. Postoperative lumbar drainage is avoided, and it is used only when the dura defect is large and can not be closed in a watertight fashion.

Postoperative Care Extubation is carried out only after the patient is completely awake to avoid aspiration caused by a dysfunction of caudal cranial nerves. A nasal-gastric tube is placed in all patients. Swallowing function must be controlled. A tracheostomy is performed when the patient experiences swallowing difficulty with recurrent aspiration.

RESULTS Radical tumor resection was achieved in 79 (74%) of all patients studied and in 89% of benign tumors (Table 1). Fortynine paragangliomas (80%) were complete excised. Three of the patients with paragangliomas presented with a recurrence of a lesion with a mean postoperative follow-up of 3 years. These cases were reoperated. Total resection was not possible in 12 patients with paragangliomas. Subtotal removal was performed in eight cases owing to the infiltration of lower cranial nerves (patients with good preoperative function) and in four owing to the infiltration of the cranial nerves, brainstem, and bone structures (three of these patients had undergone previous operations elsewhere). Four paragangliomas were histologically malignant. Chondrosarcomas, chordomas, and malignant tumors could not be totally resected owing to extensive infiltration of cranial nerves, dura, and bone. Postoperative radiotherapy was performed in cases of malignant and invasive lesions. The complications are demonstrated in Table 2. The most frequent and also more dangerous complication was a new deficit of lower cranial nerves. Ten patients (9.4%) developed lower cranial nerve palsy, which was permanent in six cases. Tracheotomy was performed in three of these patients. Facial nerve and cochlear nerve paralysis was observed in eight patients (7.5%). Facial nerve function returned spontaneously in three. In five patients, the facial nerve was resected owing to tumor infiltration and reconstruction was performed with nerve grafts (greater auricular nerve) or Cranial Nerve XII–VII anastomosis (one patient). Functional recovery of the facial nerve was Grade III in four patients and Grade IV in another (12). CSF leakage occurred in four patients (3.7%). These CSF

TABLE 2. Surgical complicationsa New cranial nerve deficits VII VIII IX, X, XI CSF leak

4

Hemiparesis

1

Mortality FIGURE 10. A, intradural exposure of a JF paraganglioma. B, total removal of the lesion with preservation of the caudal cranial nerves (Caudal C.N.). VI, VII, and VIII, cranial nerves.


8 (3 transient) 8 10 (4 transient)

a

4 (3.7%)

CSF, cerebrospinal fluid.


TUMORS

fistulae were treated with reoperation (one patient) and lumbar drainage (three patients). Three of these patients developed meningitis. Four patients (3.7%) died after surgery. Causes of death were: pulmonary embolism (one patient), aspiration pneumonia complicated with septicemia (two patients), and large cervical hematoma causing tracheal deviation and hypoxia (one patient). The patient with pulmonary embolism was a 65-year-old woman who developed massive pulmonary embolism 3 days after surgery. A lesion of preoperative functioning lower cranial nerves caused aspiration pneumonia and fatal septicemia in two cases. The fourth patient experienced a large cervical hematoma, caused by bleeding from the ligated internal jugular vein 2 days after surgery. Intubation of this patient was difficult, but the hematoma was immediately evacuated. The patient died 2 weeks later, secondary to complications of brain hypoxemia and septicemia. Double ligature of the internal jugular vein should always be performed to avoid this complication. Functional outcome was mostly affected by postoperative paralysis of caudal cranial nerves (nine patients) and hemiparesis (one patient). Preoperative Karnofsky grade was 100 in 86 patients, 90 in 9 patients, 80 in 9 patients, and 70 in 2 patients. Postoperatively, there were 80 patients with a Grade 100, 10 patients with a Grade 90, 8 patients with a Grade 80, 3 patients with a Grade 70, and 1 patient with a Grade 60.

ILLUSTRATIVE CASES Paraganglioma A 45-year-old woman complained of right side pulsatile tinnitus for 2 years before admission to our clinic. ENT examinations were normal and no radiological examination was performed. The symptoms increased in intensity, and she developed right side hearing loss. CT and MRI examinations revealed a large tumor in the JF, posterior fossa, ear, and cervical region (Fig. 1). The neurological examination at the time of admission showed a left side deafness and hypesthesia of the left nasopharynx. The tumor was totally removed using the surgical approach described above (Fig. 1). No postoperative additional deficit was observed.

Schwannoma In August 1997, a 62-year-old woman was admitted to our clinic presenting with a several-month history of swallowing difficulty and tinnitus on the left side. The neurological examination showed decreased hearing and paralysis of Cranial Nerves IX and X on the left side. MRI revealed a large enhancing cystic JF lesion with extensions to the posterior fossa and cervical region (Fig. 2). Total removal of the tumor without additional neurological deficits was accomplished (Fig. 2).

Meningioma A 12-year-old girl presented with an 8-month history of hoarse voice and swallowing difficulty. At the time of admission, the neurological examination revealed paralysis of the right Cranial Nerves IX and X. MRI showed a large enhancing tumor in the right JF with dura tail (Fig. 3). This tumor was totally resected. The postoperative course

NEUROSURGERY

OF THE JUGULAR

FORAMEN

was uneventful, and the control MRI examination 2 years and 5 months after operation showed no recurrence (Fig. 3).

DISCUSSION In 1941, Guild (11) described carotid body-like structures normally occurring in the temporal bone and named them glomus jugulare bodies. They are situated in the following sites: 1) in the adventitia of the jugular bulb beneath the floor of the middle ear, 2) in the bony walls of the tympanic canals related to the tympanic branches of the glossopharyngeal and vagus nerves, and 3) in the bone of the promontory, close to the mucosal lining of the middle ear (24). The arterial blood supply to these bodies comes from the ascending pharyngeal artery through its inferior tympanic branch. Glomus tissue is also found in the ciliary ganglion, ganglion nodosum of the vagus nerve and in the walls of the large arteries (4). Histologically, these bodies are similar to the glomus caroticum and the glomus aorticum. In April 1942, Rosenwasser (33, 34) operated on a patient with a bleeding mass which arose in the middle ear and protruded from the ear canal. Histologically, this tumor was identical to the benign carotid body tumors. In 1945, Rosenwasser (33) was the first to recognize the relationship between these tumors of the middle ear and the glomus jugulare bodies. Accumulations of chemoreceptor cells and nonchromaffin-staining paraganglion cells are found in the head and neck region. These structures are developed from the neural crest region during embryogenesis (39, 42). The JF presents a complex bony and neurovascular anatomy. Several anatomic studies have been performed, but the surgical anatomy of this region remains poorly understood (17, 22). The bony formation and the shape of the JF associated with numerous cranial nerves and venous channels passing through it make anatomic surgical comprehension difficult. Precise knowledge of the anatomy of the related regions (temporal bone, posterior fossa, and high cervical region) is necessary to approach lesions in the JF. The most frequent tumor arising in this region is paraganglioma. And, the most frequent locations of paragangliomas are the jugular bulb region (glomus jugulare), the middle ear (glomus tympanicum), and along the course of the vagus nerve (glomus vagale). Other tumors affecting the jugular foramen are meningiomas, schwannomas of the lower cranial nerves, chondrosarcomas, and other less frequent lesions. Diagnosis of JF tumors is usually made by ENT surgeons because the most frequent complaints of these patients are related to symptoms affecting hearing and swallowing. Patients with paragangliomas usually present with initial symptoms of hearing loss and tinnitus. Growth of the lesion will cause facial paralysis, polypoid mass in the external auditory canal, vertigo, hoarseness, paralysis of the tongue, and, in more advanced cases, cerebellar symptoms and hemiparesis. Neurosurgeons usually see patients with large lesions in the posterior fossa. Paralysis of lower cranial nerves is often an initial symptom of other tumors arising in the JF. In this series, all patients with meningiomas presented with lower cranial


RAMINA

ET AL.

nerve deficits. Clinical signs and symptoms may not accurately indicate the extension of the lesion. The treatment of choice for benign JF tumors is radical removal (8, 10, 14, 30, 32, 35). Controversy exists about the role of surgery for large paragangliomas with intracranial extension (4, 8). Complete resection with the preservation of the cranial nerves and vessels remains a challenge in many cases. Paragangliomas of the temporal bone can invade the cranial nerves. These nerves may present normal function despite infiltration, and total resection is only possible with sacrifice of these nerves (36). Deep location, hypervascularization, involvement of cranial nerves and vessels, infiltration of the brainstem, bone infiltration at cranial base, and large extension within the posterior fossa are the main difficulties for surgical resection of these lesions. The preoperative work-up of these patients must include a complete otological and neurological examination, audiological and vestibular testing, CT, MRI, MRA, and DSA. Balloon test occlusion is performed if the ICA is involved or encased. Preoperative embolization for well vascularized lesions, as large paragangliomas and some meningiomas, is very useful to reduce bleeding and surgical time (25). If the ICA is infiltrated by a benign tumor in young patients, reconstruction of the ICA (saphenous vein or radial artery high flow shunt) is performed only when total removal of the lesion is anticipated. Adequate tumor exposure and cranial base reconstruction is necessary to avoid postoperative complications. The development of multidisciplinary cranial base teams combining the expertise of neurosurgeons and ENT surgeons allows a patient the best chance of radical removal with preservation of the involved structures. CSF leakage after resection of large JF tumor is common and may be a serious complication (15, 18, 41). Techniques for reconstruction of surgical defect include an abdominal fat graft or the rotation of local and distant pedicled muscle flaps and free muscle flaps vascularized with microsurgical vessel anastomosis (1, 8, 16, 28). These procedures have disadvantages, and postoperative CSF leakage is not uncommon. Reconstruction with abdominal fat is used frequently, but it requires an additional skin incision and the fat tissue is not vascularized. Foreign body reaction, compression of the brainstem (6), and cases of lipoid meningitis are described in the literature (13, 31). Regional muscle flap rotation increases surgical time, needs additional incisions, and may produce poor cosmetic results (2, 9, 27). Free muscle flaps vascularized with microsurgical techniques increase surgical time and the risk of infection, require an additional surgical team, and have higher morbidity in elderly patients (2, 5, 26). Postoperative lumbar drainage is used by many authors (8, 37). This procedure may have serious morbidity (38). The cranial base reconstruction technique presented in this paper has been used since 1987 (29) and has several advantages when compared with the other approaches. This technique is easy to perform, uses two vascularized flaps, can be used for both small and large defects, causes no additional deficits, is effective in CSF leakage prevention, reduces the need of post-


operative lumbar drainage, and the cosmetic results are very good. In most patients, morbidity is related to new deficits of lower cranial nerves. When these nerves are not infiltrated, their identification and dissection in the neck and at the brainstem is helpful to preserve them. Lesion of these nerves may cause aspiration pneumonia that can be a very serious complication. Two patients in this series died from aspiration pneumonia. Tracheotomy should be performed as early as possible if clinical signs of persistent aspiration are present. Death of one patient was caused by a large hematoma in the neck with deviation of trachea and respiratory insufficiency. Postoperative bleeding from the external jugular vein or another large vein may be the source of hemorrhage. Suture or ligature of these vessels should be performed to avoid such complications. Radiation therapy is recommended by some authors to treat paragangliomas because it is associated with lower morbidity of caudal cranial nerves (23, 40). The beneficial effects of radiation therapy for paragangliomas of temporal bone remains, however, uncertain (10). The effect of irradiation appears to be on the blood vessels and fibrous elements of the lesion (3, 20, 40). More than 80% tumor control is reported after radiation therapy (7, 19, 20). In our series, postoperative radiation therapy was indicated for elderly patients who are poor surgical candidates and for patients with malignant or aggressive tumors and tumor remnants in the cavernous sinus that present growth. Radiosurgery using gamma knife or a linear accelerator system may be more beneficial in reducing side-effects of irradiation. Radiation-induced neoplasm has been described after radiotherapy for benign glomus jugulare tumors (21).

CONCLUSION Paragangliomas are the most frequent tumors of the JF, followed by schwannomas, meningiomas, and chondrosarcomas. Surgical removal remains the treatment of choice and may be curative in cases of schwannomas, benign meningiomas, noninfiltrative paragangliomas, and other benign JF tumors. Large paragangliomas of the JF with intracranial extension may be radically excised through a multidisciplinary approach with preservation of lower cranial nerves. Preoperative embolization permits one-stage operation with low blood loss in most cases of paragangliomas and well vascularized tumors. Paralysis of the lower cranial nerves with dysphasia remains the most serious complication related to surgery. Delayed extubation, tracheotomy in selected cases, and early rehabilitation are very important in the postoperative management of patients with involvement of the lower cranial nerves.

REFERENCES 1. Anand V: Reconstruction in cranial base surgery, in Al-Mefty O (ed): Surgery of the Cranial Base. Boston, Kluwer Academic Publishers, 1989, pp 297–314.


TUMORS

2. Ariyan S: Pectoralis major muscle and musculocutaneous flaps, in Strauch B, Vasconez LO, Hallfindlay EJ (eds): Grabb’s Encyclopedia of Flaps. Boston, Little Brown Co., 1990, pp 512–522. 3. Brackmann DE, House WF, Terry R, Scanlan RL: Glomus jugulare tumors: Effect of irradiation. Trans Am Acad Ophthalmol Otolaryngol 76:1423– 1431, 1972. 4. Brown J: Glomus jugulare tumors revisited: A ten-year statistical follow-up of 231 cases. Laryngoscope 95:284–288, 1985. 5. Chang DW, Langstein HN, Gupta A, DeMonte F, Do KA, Wang X, Robb G: Reconstructive management of cranial base defects after tumor ablation. Plast Reconstr Surg 6:1346–1355, 2001. 6. Chen TC, Maceri DR, Levy ML, Giannotta SL: Brain stem compression secondary to adipose graft prolapse after translabyrinthine craniotomy: Case report. Neurosurgery 35:521–533, 1994. 7. Cummings BJ, Beale FA, Garrett PG, Harwood AR, Keane TJ, Payne DG, Rider WD: The treatment of glomus tumors in the temporal bone by mega voltage radiation. Cancer 53:2635–2640, 1984. 8. Fisch U: Infratemporal fossa approach for glomus tumors of the temporal bone. Ann Otol Rhinol Laryngol 91:474–479, 1982. 9. Gal TJ, Keschner JE, Futran ND, Bartels LJ, Farrior JB, Ridley MB, Klotch DW, Endicott JN: Reconstruction after temporal bone resection. Laryngoscope 108:476–481, 1998. 10. Green JD, Brackmann DE, Nguyen CD, Arriaga MA, Telischi FF, De la Cruz A: Surgical management of previously untreated glomus jugulare tumors. Laryngoscope 104:917–921, 1994. 11. Guild SR: A hitherto unrecognized structure: The glomus jugularis in man. Anat Rec 79[Suppl 2]:28, 1941 (abstr). 12. House JW, Brackmann DE: Facial nerve grading system. Otolaryngol Head Neck Surg 93:146–147, 1985. 13. Hwang PH, Jackler RK: Lipoid meningitis due to aseptic necrosis of a free graft placed during neurotologic surgery. Laryngoscope 106:1482–1486, 1996. 14. Jackson CG, Glasscock ME, Nissen AJ, Schwaber MK: Glomus tumor surgery: The approach, results and problems. Otolaryngol Clin North Am 15:897–916, 1982. 15. Jackson CG, Woods C, Drinoris PN: Glomus jugulare tumors, in Sekhar LN, Janecka IP (eds): Surgery of Cranial Base Tumors. New York, Raven Press, 1993. 16. Jones NF, Schramm VL, Sekhar LN: Reconstruction of the cranial base following tumour resection. Br J Plast Surg 40:155–162, 1987. 17. Katsuta T, Rhoton AL Jr, Matsushima T: The jugular foramen: Microsurgical anatomy and operative approaches. Neurosurgery 41:149–202, 1997. 18. Kempe LG: Glomus jugulare tumor, in Youmans JR (ed) Neurological Surgery. Philadelphia, W.B. Saunders Co., 1982, pp 3285–3298. 19. Kim JA, Elkon D, Lim ML, Constable WC: Optimum dose of radiotherapy for chemodectomas of the middle ear. Int J Radiol Oncol Biol Phys 6:815– 819, 1980. 20. Konefal JB, Pilepich MV, Spector GJ, Perez CA: Radiation therapy in the treatment of chemodectomas. Laryngoscope 97:1331–1335, 1987. 21. Lalwani AK, Jackler RK, Gutin PH: Lethal fibrosarcoma complicating radiation therapy for benign glomus jugulare tumor. Am J Otol 14:398–402, 1993. 22. Lang J: Anatomy of the jugular foramen, in Samii M, Draf W (eds): Surgery of the Skull Base. Berlin, Springer Verlag, 1989, pp 59–64. 23. Larner JM, Hahn SS, Spaulding CA, Constable WC: Glomus jugulare tumors: Long-term control by radiation therapy. Cancer 69:1813–1817, 1992. 24. Lattes R, Waltner JG: Nonchromaffin paraganglioma of the middle ear. Cancer 2:447, 1949. 25. Murphy TP, Brackmann DE: Effects of preoperative embolization on glomus jugular tumors. Laryngoscope 99:1244–1247, 1989. 26. Mustoe TA, Corral CJ: Soft tissue reconstructive choices for craniofacial reconstruction. Clin Plast Surg 22:534–554, 1995. 27. Neligan PC, Mulholland S, Irish J, Gullane PJ, Boyd JB, Gentili F, Brown D, Freemann J: Flap selection in cranial base reconstruction. Plast Reconstr Surg 7:1159–1166, 1996. 28. Netterville JL, Civantos EJ: Defect reconstruction following neurologic skull base surgery. Laryngoscope 103:55–63, 1993.

NEUROSURGERY

OF THE JUGULAR

FORAMEN

29. Ramina R, Maniglia JJ, Barrionuevo CE: Glomus jugulare tumors: Classification and treatment. Presented at the International Symposium on Cranial Base Surgery, Pittsburgh, Pennsylvania, September 13–17, 1988. 30. Ramina R, Maniglia JJ, Pedrozo AA, Clemente RS, Meneses MS: Surgical treatment of jugular foramen tumors [in German]. Zentralbl Neurochir 57(Suppl)1:47–47, 1996. 31. Ricaurte JC, Murali R, Mandell W: Uncomplicated postoperative lipoid meningitis secondary to autologous fat graft necrosis. Clin Infect Dis 30: 613–615, 2000. 32. Roberstson JT, Clark WC, Robertson JH, Gardner LG: Glomus jugulare tumors, in Youmans JR (ed) Neurological Surgery. Philadelphia, W.B. Saunders Co., 1990, ed 3, pp 3654–3666. 33. Rosenwasser H: Carotid body like tumor involving the middle ear and mastoid bone. Arch Otolaryngol 41:64–67, 1945. 34. Rosenwasser H: Glomus jugulare tumors: Part I—Historical background. Laryngoscope 62:623–633, 1952. 35. Samii M, Tatagiba M: Tumors of the jugular foramen. Neurosurg Q 6:176– 193, 1996. 36. Sen C, Hague K, Kacchara R, Jenkins A, Das S, Catalano P: Jugular foramen: Microscopic anatomic features and implications for neural preservation with reference to glomus tumors involving the temporal bone. Neurosurgery 48:838–848, 2001. 37. Shapiro AS, Scully T: Closed continuous drainage of cerebrospinal fluid via a lumbar subarachnoid catheter for treatment or prevention of cranial/ spinal cerebrospinal fluid fistula. Neurosurgery 30:241–245, 1992. 38. Snow RB, Kuhel W, Martin SB: Prolonged lumbar spinal drainage after the resection of tumors of the skull base: A cautionary note. Neurosurgery 28:880–882, 1991. 39. Spector GJ, Ciralsky R, Maisel RH: Multiple glomus tumors in the head and neck. Laryngoscope 85:1066–1075, 1975. 40. Springate SC, Weichselbaum RR: Radiation or surgery for chemodectoma of the temporal bone: A review of local control and complications. Head Neck 12:303–307, 1990. 41. Watkins LD, Mendoza N, Cheesman AD, Symon L: Glomus jugulare tumours: A review of 61 cases. Acta Neurochir (Wien) 130:66–70, 1994. 42. Zak FG: An expanded concept of tumors of glomic tissue. N Y State J Med 54:1153–1165, 1954.

COMMENTS

R

amina et al. present a series of 100 consecutive patients operated on for jugular foramen tumors. The most prevalent tumor was paraganglioma (56%). They achieved total tumor resection in 73% of the patients, with low morbidity and mortality. They describe a new technique of reconstruction of the cranial base with three myofascial layers. With this technique they had only 4% of cerebrospinal fluid leak, without using lumbar drainage routinely. The facial nerve is left in the canal unless it is infiltrated by the tumor. Permanent facial paralysis occurred in five cases. Preoperative embolization was used in most cases of paragangliomas. Paragangliomas are slow-growing tumors. A long period of follow-up is necessary to rule out any recurrence. It is not clear in this article how long the follow-up was in this series. In our opinion, radiosurgery is the treatment of choice for tumor remnants. Jair L. Raso Evandro de Oliveira São Paulo, Brazil

I

n this article, Ramina et al. have presented their extensive experience with tumors involving the jugular foramen, including paragangliomas, schwannomas, chordomas, meningiomas, and other malignancies. Although their intent was to achieve complete resection, only subtotal removal was achieved in 12 of 57 patients with glomus tumors.


RAMINA

ET AL.

In our previous publications, the occasional need for tumorinvaded internal carotid artery replacement with vein or arterial grafts, and the occasional need for jugular bulb-sigmoid sinus bypass with vein graft when the tumor involved sinus is dominant, was emphasized (1, 3). Schwannomas of the jugular foramen are much easier to remove, and lower cranial nerve function can be well preserved in these patients (2). The acute paralysis of the lower cranial nerves and the paralysis of the facial nerve (albeit with good recovery) are the greatest morbidity in these patients. Facial nerve results have improved dramatically in many series, owing to the technique of leaving the nerve in situ during the resection, or mobilizing the nerve with the digastric muscle. The results with reference to the lower cranial nerves have improved owing to the use of lower cranial nerve monitoring. When paralysis of the lower cranial nerves occurs, early vocal cord medialization can obviate the need for a tracheostomy in most patients. There is definitely a role for radiosurgery for treatment of paragangliomas and meningiomas in some of these patients, especially when they are older or have absolutely no cranial nerve deficits. Laligam N. Sekhar Seattle, Washington

1. Patel SL, Sekhar LN, Cass SP, Hirsch BE: Combined approaches for resection of glomus jugulare tumors: A review of 12 cases. J Neurosurg 80:1026–1038, 1994. 2. Sekhar LN, Sarma S, Schessel D: Non-vestibular schwannomas of the brain: A 7 year experience. Neurosurgery 50:437–449, 2002. 3. Sekhar LN, Tzoridis FN, Bejjani GK, Schessel D: Saphenous vein graft bypass of the sigmoid sinus and jugular bulb during the removal of glomus jugulare tumors. J Neurosurg 86:1036–1041, 1997.

T

he authors report about the microsurgical treatment and cranial base reconstruction in a large series of 100 tumors of the jugular foramen, most of them paragangliomas (57%), schwannomas (16%), and meningiomas (10%). Total tumor resection was achieved in 73% of the lesions. The authors rightly point out the importance of an interdisciplinary management in these complex lesions, including preoperative embolization and internal carotid artery-occlusion testing if it is encased by the lesion. Combining surgical expertise from specialized ear, nose, and throat surgeons and neurosurgeons in planning and execution of surgery is mandatory for successful treatment. Postoperative care includes special attention to swallowing difficulties with prolonged nasogastric tube feeding if necessary. Still, the authors document two cases of pneumonia resulting from aspiration with fatal outcome. Postoperative radiation therapy might follow in subtotally resected lesions, preferably by stereotactic radiation to reduce side effects. We have to point out that ligation of the sigmoid sinus, as described in the surgical procedure section, is not always necessary, especially in the case of schwannomas located in the jugular foramen. The surgical strategy should be tailored to the radiologically documented extent of the lesion. From our experience, we recommend the use of sural nerve graft for facial nerve reconstruction, if necessary, rather than greater auricular nerve grafts. Greater auricular nerve grafting results in more disabling hypesthesias than sural nerve resection. Regarding the plastic closure of the resulting defect, we experienced good results in a large series of patients in recent years using one-piece fat grafts attached by fibrin glue with a combination of careful lumbar drainage. Madjid Samii Wolf Lüdemann Hannover, Germany

Congress of Neurological Surgeons/American Association of Neurological Surgeons Joint Section Chairmen Cerebrovascular Surgery: Philip E. Stieg, New York, New York Disorders of the Spine and Peripheral Nerves: Gerald E. Rodts, Jr., Atlanta, Georgia History of Neurological Surgery: Dennis E. McDonnell, LaCrosse, Wisconsin Neurotrauma and Critical Care: Alex B. Valadka, Houston, Texas Pain: Oren Sagher, Ann Arbor, Michigan Pediatric Neurological Surgery: Andrew D. Parent, Jackson, Mississippi Stereotactic and Functional Neurosurgery: G. Rees Cosgrove, Boston, Massachusetts Tumors: Raymond Sawaya, Houston, Texas

